The inoculation of plants with plant-growth-promoting rhizobacterium has been an effective strategy for enhancing plant salt tolerance to diminish the loss of agricultural productivity caused by salt stress; however, the signal transmitted from bacteria to the plant under salt stress is poorly understood. In this study, the salt tolerance of Arabidopsis thaliana and Zea mays was enhanced by inoculation with Bacillus amyloliquefaciens SQR9. Using dialysis bags with different molecular weight cutoffs, we sorted through the molecules secreted by SQR9 and found that spermidine is responsible for enhancing plant salt tolerance. An SQR9 ΔspeB mutant deficient in spermidine production failed to induce plant salt tolerance. However, the induction of plant salt tolerance was disrupted by mutating genes involved in reduced glutathione (GSH) biosynthesis and the salt overly sensitive pathway in Arabidopsis. Using quantitative real-time polymerase chain reaction, this study demonstrated that spermidine produced by SQR9 leads to increased glutamine synthetase and glutathione reductase gene expression, leading to increased levels of GSH, which is critical for scavenging reactive oxygen species. SQR9-derived spermidine also upregulates the expression of NHX1 and NHX7, which sequesters Na+ into vacuoles and expels Na+ from the cell, thereby reducing ion toxicity.